The influence of heavy metal stress on the evolutionary transition of teosinte to maize

Maize originated from teosinte parviglumis following a subspeciation event occurred in volcanic regions of Mesoamerica. The elucidation of the phenotypic changes that gave rise to maize have focused on the direct consequences of domestication, with no insights on how environmental factors could have influenced specific gene function and human selection. We explored the impact of heavy metal (HM) stress by exposing both subspecies to sublethal concentrations of copper and cadmium. We also assessed the genetic diversity of loci encompassing three HM response genes affected by domestication: ZmHMA1 , ZmHMA7 – encoding for heavy metal ATPases of the P1 _b family-, and ZmSKUs5, encoding a multicopper oxidase. ZmHMA1 and ZmSKUs5 map in the short arm of chromosome five, in a genomic region containing multiple linked QTLs with pleiotropic effects on domestication. A genomic analysis of the full chromosome shows that their loci show strong positive selection as compared to previously identified domestication genes. Exposure of teosinte parviglumis to HM stress results in a plant architecture reminiscent of extant maize, and upregulation of Teosinte branched1 ( Tb1 ) in the meristem. ZmHMA1 and ZmHMA7 are expressed throughout development and respond to HM stress in both subspecies. ZmHMA1 is mainly involved in restricting plant height and optimizing the number of female inflorescences and seminal roots. Our results suggest that HM stress acted on specific ATPases involved in homeostasis, giving rise to phenotypic variants that were identified and selected by humans during domestication.